研究報告

中華昆蟲 20 : 13-21 ( 2000) Chinese J. Entomol. 20: 1 3 - 21 (2000)

Prior Experience Affects the Oviposition Behavior in (L.) ( Hymenoptera: Evaniidae)

Chin-Chang Yeh and Chi-Chang Huang Department of Entomology, National Chung- Hsing University Taichung, Taiwan 402, R.O.C. Cheng-Shing Lin* Department of Zoology, National Museum of Natural Science Taichung, Taiwan 404, R.O.C.

ABSTRACT

We evaluated the effect of prior ovipositional experience on the oviposition of Evania appendigaster (L.) (Hymenoptera: Evaniidae). Prior experience reduced the total time of the oviposition sequence; the preoviposition quiescent stage occupied most of the time for oviposition and was the most important plastic behavioral stage. If oviposition experience was withheld for more than three days, females seemed to forget what they had learned and acted as naive females. Booster experience did not decrease total time to finish the sequence of oviposition behavior.

Key words: Evania appendigaster, Periplaneta americana, behavior, learning.

Introduction the habitat alone (Wardle and Borden, 1985; 1991). In four species of aphidiid wasps, prior The ensign wasp Evania appendigaster oviposition experience was found to affect is a solitary parasitoid of . It can host selection (Chow and Mackauer, 1992). be found in temperate and subtropical Oviposition experience also reduced the areas (Townes, 1949). Its hosts include approach time of Ooencyrtus kuvanae; the Periplaneta americana, P. australasiae, P. more experience in oviposition the wasp brunea, Blatta orientalis, Cutilia soror, and had acquired the less oviposition time rhombifolia (Lebeck, 1991). needed (Lee and Lee, 1989; Lee et al., 1989). Its developmental period lasts for about Females with oviposition experience on a 38-40 days, and the longevity of adults is host pupa are more likely than naive about 13 to 15 days in the laboratory (Yeh females to walk upwind in kairomone- and Mu, 1994a). E. appendigaster shows a laden air and to do so more rapidly ( Carde fixed action pattern of oviposition behavior and Lee, 1989). Females of the polyph- on the ootheca of P. americana. Its agous ichneumonid parasitoid Exeristes oviposition sequence can be divided into roborator demonstrate associative learning seven steps: (1) host contact (with antennal by responding with ovipositor probes into drumming), (2) ovipositor extension and

*Correspondence address e-mail:[email protected] Prior Experience Affects Oviposition Behavior in E. appendigaster 13 tapping, (3) preoviposition quiescence, (4) three eggs, one each on the 1st, 2nd, and drilling, (5) ovipositing, (6) withdrawal, 5th days, respectively (1-2-5); (4) 4th and (7) departure. experiment: oviposition of three eggs, one Females are attracted to host ootheca. each on the 1st, 2nd, and 7th days, They contact the ootheca by antennal respectively (1-2-7); (5) 5th experiment: drumming, then either fly away or stay on oviposition of three eggs, one each on the it. The wasps extend the ovipositor and tap 1st, 2nd, and 9th days, respectively (1-2-9); the ootheca surface. It takes about 10 (6) 6th experiment: oviposition of 2 eggs, minutes for the wasps to locate the “right one each on the 1st, and 4th days, spot”, and complete the preoviposition respectively (1-4); (7) 7th experiment: ovi- quiescent stage. Females move their ab- position of three eggs, one on the 1st day domen up and down, drill the ovipositor and two consecutive ovipositions on the 5th into the ootheca, pull it out, and drill day (1-5-5); (8) 8th experiment: oviposition repeatedly, looking for a good position. of one egg on the 1st day and two They then just sit on ootheca and lay eggs consecutive ovipositions on the 6th day followed by withdrawal of the ovipositor (1-6-6); (9) 9th experiment: oviposition of and departure. The effects of prior ovi- one egg on the 1st day, and two consecutive position experience on the oviposition be- ovipositions on the 8th day (1-8-8). havior of the ensign wasp were tested in Wasps were exposed to consecutive the laboratory. In this paper, we define oviposition experiences to determine if oviposition as actual egg laying by females, prior experience reduces the time of ovi- oviposition behavior as all seven behav- position. Wasps with prior oviposition ex- ioral steps, and an oviposition event as a perience were held without additional single sequence of oviposition behavior. experience for one day (1-2-3), three days (1-2-5) (1-4), five days (1-2-7), or seven Materials and Methods days (1-2-9), or in other experiments, for four days (1-5-5), five days (1-6-6), or seven Rearing of P. americana and E. days (1-8-8) followed by consecutive ovi- appendigaster was performed using the positions, to determine how long experi- methods of Yeh and Mu (1994a, b). Ooth- ence could be withheld, and if booster ecae used in the experiments were depo- experience could increase the oviposition sited by American within 24 h efficiency and shorten the time of the of the experiments. A single naive female oviposition sequence. Each experiment was (i.e., without previous oviposition experi- done with eight replications. All experi- ence) ensign wasp (three days old and ments were carried out in a walk-in gro- mated at the day after emergence) was wth chamber (180 X 180 X 180 cm) at released in a lid-covered plastic cup (9 cm 26-28℃, 70-90% RH, with a L:D = 12:12 dia. X 5 cm) containing one ootheca, and photoperiod. the wasp oviposition behavior was obser- For data analysis, we used the split- ved. Detailed oviposition behavior and plot design. In the main plot, ovipsoitional total oviposition times were recorded with event treated as the treatment of one a V8 video camera. factor and the female as a block, arranged The following experiments were con- in a randomized complete block design. ducted: (1) 1st experiment: consecutive The oviposional stages were treated as ovipositions of three eggs on three oothecae treatments of the second factor, and were on the 1st day (indicated as 1-1-1); (2) 2nd assigned to subplots within each main plot. experiment: oviposition of three eggs, one Significance between treatments was eva- each on 1st, 2nd, and 3rd days, respectively luated and followed by range test (SAS, (1-2-3); (3) 3rd experiment: oviposition of 1988). All values are presented as mean ±

14 中華昆蟲第二十卷第一期 SD. between experienced and naive wasps. The stage of quiescent was significantly longer Results than the other stage both in the experi- enced wasps and the naive wasps. The Wasps were exposed to consecutive stage of oviposition was the next longer oviposition experiences on the same day stage in both experienced and naive wasps. (1-1-1) to determine if prior experience If booster experiences took place reduced the time of oviposition (Table 1). within three days, the total time to finish The total time needed to finish the the sequence of oviposition behavior was sequence of behavior was significantly significantly shorter in experienced wasps shorter for experienced than for naive (OEII) (i.e., 1-1, 1-2, 1-4) (Tables 1, 2, 4, 5, wasps. Time spent in the preoviposition and 6) than in naive wasps. In addition, quiescent stage and the withdrawal stage the preoviposition quiescent stage was was significantly shorter in experienced significantly shorter in experienced than wasps than in naive wasps. The total time in naive wasps. But, when oviposition spent by experienced wasps to finish the experience was withheld for more than sequence of behavior was not significantly three days (i.e., 1-5, 1-6, 1-8) (Tables 7, 8, different between oviposition events II and and 9), the total time to finish the sequence III (OEII & OEIII). There were significant of oviposition behaviors were not signi- differences in oviposition behavioral stages ficantly different between experienced and

Table 1. Mean ovipositional time (sec.) ± SD of 3 consecutive ovipositions within 1 day (1-1-1) in E. appendigaster Oviposition Mean ovipositional time (sec.) ± SD (n = 8) Behavior OE I 1) OE II OE III 1. Host contact 16.6 ± 5.6a 2) 19.4 ± 8.5a 6.3 ± 7.8a 2. Tapping 93.6 ± 66.7a 42.5 ± 13.5a 70.1 ± 35.1a 3. Quiescence 560.5 ± 188.6a 342.6 ± 166.7b 375.4 ± 156.6b 4. Drilling 95.9 ± 86.9a 39.1 ± 27.8a 101.3 ± 63.9a 5. Oviposition 173.3 ± 40.3a 172.9 ± 69.7a 142.0 ± 20.7a 6. Withdrawal 71.5 ± 12.4a 55.6 ± 8.3a 46.6 ± 10.4a Total 1011.4 ± 299.2a 672.1 ± 168.3b 751.7 ± 169.3b 1.) OE = ovipositional event (I, II, III). 2.) Means in the same row followed by the same letter are not significantly different by Fisher ’s LSD test (p < 0.05 ) .

Table 2. Mean ovipositional time (sec.) ± SD of 3 ovipositions with 1-day intervals (1-2-3) in E. appendigaster Oviposition Mean ovipositional time (sec.) ± SD (n = 8) behavior OE I (1st d) 1) OE II (2nd d) OE III (3rd d) 1. Host contact 28.5 ± 8.8a 2) 16.0 ± 7.9b 19.0 ± 10.6b 2. Tapping 141.8 ± 92.1a 76.3 ± 59.6b 57.3 ± 29.2b 3. Quiescence 618.1 ± 258.8a 411.9 ± 190.1b 359.8 ± 162.1b 4. Drilling 68.8 ± 49.2a 25.0 ± 8.0a 36.9 ± 27.5a 5. Oviposition 193.8 ± 106.1a 157.0 ± 42.5a 144.0 ± 44.2a 6. Withdrawal 63.2 ± 19.8a 49.1 ± 14.9a 52.8 ± 12.5a Total 1114.2 ± 290.8a 735.3 ± 175.6b 669.8 ± 202.6b 1.) OE = ovipositional event (I, II, III). 2.) Means in the same row followed by the same letter are not significantly different by Fisher ’s LSD test (p < 0.05 ) .

Prior Experience Affects Oviposition Behavior in E. appendigaster 15 Table 3. Mean ovipositional time (sec.) ± SD of 3 ovipositions with 1-day and 3-day intervals (1-2-5) in E. appendigaster Oviposition Mean ovipositional time (sec.) ± SD (n = 8) behavior OE I (1st d) 1) OE II (2nd d) OE III (3rd d) 1. Host contact 29.1 ± 24.1a 2) 19.3 ± 14.1a 15.4 ± 4.4a 2. Tapping 129.9 ± 124.2a 32.3 ± 11.4a 76.3 ± 44.7a 3. Quiescence 667.7 ± 262a 481.9 ± 121b 449.3 ± 129.9b 4. Drilling 101.1 ± 75a 38.1 ± 27.2a 49.3 ± 34.7a 5. Oviposition 165.4 ± 16.4a 140.1 ± 36.9a 170.7 ± 55.4a 6. Withdrawal 58.9 ± 14a 51.3 ± 10.2a 55.9 ± 6.3a Total 1152.1 ± 259.9a 763 ± 244.4b 816.9 ± 282.1b 1.) OE = ovipositional event (I, II, III). 2.) Means in the same row followed by the same letter are not significantly different by Fisher ’s LSD test (p < 0.05 ) .

Table 4. Mean ovipositional time (sec.) ± SD of 3 ovipositions with 1-day and 5-day intervals (1-2-7) in E. appendigaster Oviposition Mean ovipositional time (sec.) ± SD (n = 8) behavior OE I (1st d) 1) OE II (2nd d) OE III (3rd d) 1. Host contact 20.8 ± 6.1a 2) 14.6 ± 3.3a 16 ± 4.6a 2. Tapping 172.3 ± 90.8a 63.3 ± 39.5b 76.8 ± 34.8b 3. Quiescence 562.3 ± 143.4a 385.8 ± 102.3b 589.3 ± 102.2a 4. Drilling 47.3 ± 37.8a 22.1 ± 8a 37.1 ± 21.3a 5. Oviposition 161.9 ± 83.3a 134.4 ± 23.4a 197.4 ± 95.5a 6. Withdrawal 56.3 ± 9.7a 45.8 ± 6.9a 60 ± 11.6a Total 1020.9 ± 138.4a 666 ± 146.1b 976.6 ± 169.2a 1.) OE = ovipositional event (I, II, III). 2.) Means in the same row followed by the same letter are not significantly different by Fisher ’s LSD test (p < 0.05 ) .

Table 5. Mean ovipositional time (sec.) ± SD of 3 ovipositions with 1-day and 7-day intervals (1-2-9) in E. appendigaster Oviposition Mean ovipositional time (sec.) ± SD (n = 8) behavior OE I (1st d) 1) OE II (2nd d) OE III (3rd d) 1. Host contact 45.6 ± 21.2a 2) 33.6 ± 22.1a 24.9 ± 18a 2. Tapping 77 ± 48.9a 85.3 ± 71.9a 58 ± 36.3a 3. Quiescence 822 ± 298.4a 385.6 ± 105.3b 731.9 ± 205.3a 4. Drilling 68.3 ± 29.1a 37 ± 13.1a 86.4 ± 74.1a 5. Oviposition 183.7 ± 61.1a 143.1 ± 42.1a 165.6 ± 53.9a 6. Withdrawal 58.6 ± 16.6a 59 ± 11.8a 72 ± 11.1a Total 1255.2 ± 380.7a 743.6 ± 164.7b 1138.8 ± 176.4a 1) OE = ovipositional event (I, II, III). 2) Means in the same row followed by the same letter are not significantly different by Fisher ’s LSD test (p < 0.05). naive wasps, and the quiescent period was followed by three-day break (1-2-5) (Table 3) not significantly shorter either. experiments, the total times to finish the For same day (1-1-1) (Table 1), consecutive sequence of oviposition behavior of experienced day (1-2-3) (Table 2) and consecutive day wasps in OEIII and in OEII were not

16 中華昆蟲第二十卷第一期 Table 6. Mean ovipositional time (sec.) ± SD of 2 ovipositions with 3-day interval (1-4) in E. appendigaster Oviposition Mean ovipositional time (sec.) ± SD (n = 8) behavior OE I (1st d) 1) OE II (2nd d) 1. Host contact 19.8 ± 8.5a 2) 18.8 ± 12.3a 2. Tapping 77 ± 37.3a 85.3 ± 46.8a 3. Quiescence 692.9 ± 213.7a 428.5 ± 245.6b 4. Drilling 93 ± 91.9a 30 ± 15.1a 5. Oviposition 157.4 ± 44.1a 230.3 ± 174.2a 6. Withdrawal 59 ± 11.2a 51.5 ± 10.2a Total 1099.1 ± 225.8a 844.4 ± 234b 1) OE = ovipositional event (I, II). 2) Means in the same row followed by the same letter are not significantly different by Fisher ’s LSD test (p < 0.05).

Table 7. Mean ovipositional time (sec.) ± SD of 3 ovipositions with 4-day interval followed by consecutive ovipositions (1-5-5) in E. appendigaster Oviposition Mean ovipositional time (sec.) ± SD (n = 8) behavior OE I (1st d) 1) O E II (2nd d) OE III (3rd d) 1. Host contact 21.9 ± 6.8a 2) 16.9 ± 4.8a 16.8 ± 3.5a 2. Tapping 101.9 ± 52.8a 66.1 ± 14.4a 59.0 ± 32.6a 3. Quiescence 592.8 ± 149.6a 558.6 ± 122.9a 409.6 ± 102.9b 4. Drilling 84.6 ± 76.8a 54.1 ± 33.7a 66.5 ± 32.4a 5. Oviposition 183.4 ± 74.4a 178.5 ± 42.4a 147.6 ± 32.9a 6. Withdrawal 64.3 ± 13.9a 60.9 ± 9.5a 55.9 ± 6.9a Total 1048.9 ± 165.9a 935.1 ± 119.6a 755.4 ± 119.4b 1) OE = ovipositional event (I, II, III). 2) Means in the same row followed by the same letter are not significantly different by Fisher ’s LSD test (p < 0.05). significantly different. Booster experience for The total times needed to complete the more than three days (1-2-7, 1-2-9) (Tables 4 and oviposition sequence were consistent in 5), resulted in significantly longer total times to naive ensign wasp females. Naive wasps finish the sequence of OEIII than of OEII. The followed the seven-step oviposition beha- preoviposition quiescent stage of wasps in OEII vior patterns, and times spent in preovi- was significantly shorter than in OEI. There were position quiescent stage were similar to no significant differences in total time between those reported in the study by Yeh and Mu OEIII and OEI. Booster experiences on the same (1994b). The experienced ensign wasp day, after four, five, or seven days (1-5-5, 1-6-6, females also followed the same pattern of and 1-8-8) (Tables 7, 8, and 9) resulted in oviposition behavior. significantly shorter total times for OEIII than The postoviposition departure stage for OEII. The preoviposition quiescent stage of was not mentioned in this study because wasps for OEIII was significantly shorter than the wasps continuously stayed in the cage that for OEII. for another oviposition. Time to finish the sequence of oviposition behavior is influ- Discussion enced by the age of the oothecae (Yeh and Mu, 1994b). In order to diminish variation,

Prior Experience Affects Oviposition Behavior in E. appendigaster 17 Table 8. Mean ovipositional time (sec.) ± SD of 3 ovipositions with 5-day interval followed by consecutive ovipositions (1-6-6) in E. appendigaster Oviposition Mean ovipositional time (sec.) ± SD (n = 8) behavior OE I (1st d) 1) OE II (2nd d) OE III (3rd d) 1. Host contact 18.3 ± 9a 2) 16.9 ± 4.2a 14.9 ± 5a 2. Tapping 85.4 ± 70a 75.8 ± 46.1a 73.4 ± 33a 3. Quiescence 643.9 ± 266.4a 586.4 ± 89.7a 393.5 ± 104.8b 4. Drilling 33.4 ± 20.3a 45.4 ± 39a 28.3 ± 9.3a 5. Oviposition 144.9 ± 29.5a 168.8 ± 67a 131.2 ± 27.3a 6. Withdrawal 58.8 ± 18.2a 52.9 ± 141.6a 53.0 ± 11.1a Total 984.7 ± 209.2a 946.2 ± 141.6a 694.3 ± 140.2b 1) OE = ovipositional event (I, II, III). 2) Means in the same row followed by the same letter are not significantly different by Fisher ’s LSD test (p < 0.05).

Table 9. Mean ovipositional time (sec.) ± SD of 3 ovipositions with 7-day interval followed by consecutive ovipositions (1-8-8) in E. appendigaster Oviposition Mean ovipositional time (sec.) ± SD (n = 8) behavior OE I (1st d) 1) OE II (2nd d) OE III (3rd d)

1. Host contact 23.9 ± 16.1a 2) 27.5 ± 22a 22.3 ± 7.2a 2. Tapping 93.6 ± 66.7a 42.3 ± 13.5a 70.1 ± 35.1a 3. Quiescence 562.5 ± 213.8a 446.6 ± 156.3a 293.8 ± 86.4b 4. Drilling 69.9 ± 54a 58.9 ± 44.4a 42.9 ± 33.6a

5. Oviposition 164.8 ± 43.6a 198.4 ± 179.3a 130.6 ± 24.4a 6. Withdrawal 63.4 ± 2.7a 66.3 ± 12.7a 54.5 ± 19.7a Total 978.1 ± 285.8a 840 ± 188.9a 614.2 ± 115.3b 1) OE = ovipositional event (I, II, III). 2) Means in the same row followed by the same letter are not significantly different by Fisher ’s LSD test (p < 0.05). three-day-old ensign wasps and 24-h-old Arthur (1971) demonstrated learning oothecae were used. of novel odors by the ichneumoid Nemeritis Little evidence of learning was found canescens. Vinson et al. (1966), and Wardle in our study, but the observed result of and Borden (1988) found similar associ- ovipositing experience is consistent with ations. The physiological processes behind some definition of learning, e.g., learning associative learning have not yet been as a “change in behavior with experience” explained. Associative learning is not li- (Papaj and Prokopy, 1989). Experienced mited to olfactory stimuli, as parasitoids females learn to recognize the right ooth- are also able to link visual and mech- ecae of host and egg-laying site. anosensory stimuli (Turling et al., 1993). Parasitoid’s searching behavior can be Further studies are needed to identify the affected by experience. These experiences exact stimuli link to the associative involve contacts with specific host-derived learning in E. appendigaster. stimuli that the wasps recognize innately. Prior experience can reduce the time The wasps may also learn by associate to finish the sequence of a second ovi- learning, e.g., to ” learn to respond to position on the same day, and experience unrecognized stimuli by linking these new can be withheld up to three days. After stimuli to the contact stimuli“ (Turling et three days, the female will forget what has al., 1993). been learned and act as a naive female.

18 中華昆蟲第二十卷第一期 These ovipostion behaviors are similar to significantly different (Table 4). The host that of Ooencyrtus kuvanae, the egg contact stages of ovipositional event I (OEI) parasitoid of Lymantria dispar (Lee and and ovipositional event II (OEII) were not Lee, 1989). significantly different either (Table 7). Booster experience did not further After five days, females forgot what have decrease the total time to finish the sequ- learned and acted as inexperience females. ence of oviposition behavior. After three The tapping stage of the experienced days, females will forget the experience. In female in ovipositional event III (OEIII) a previous study, lack of continued ex- was shorter in three ovipositions with one perience for more than four days resulted day interval (Table 2). But the tapping in the forgetting what had been stages of ovipositional event I (OEI) and learned (Papaj and Prokopy, 1989) and a ovipositional event II (OEII), and oviposi- return to the naive state. tional event II (OEII) and ovipositional In general, preoviposition quiescence event III (OEIII) were not significantly occupied most of the time spent in ovi- different (Table 2). In the tapping stage, position. In some experiments, the preovi- female extended ovipositor and tapping the position host contact, tapping, and post- ootheca for location identification (Yeh and oviposition withdrawal stages of experi- Mu, 1994a). Experienced females need less enced wasps were shorter than in naive times for location identification. The tap- females. The preoviposition quiescent ping stage of experienced females was also stage is the stage where the ensign wasp shorter than that of naive females in OEII females locate the position of the ootheca (Table 4). But after five days, the tapping using the ovipositor, and it remains stages of ovipsitional event II (OEII) and quiescent for most of the time. Yeh and Mu ovipositional event III (OEIII) were not (1994b) postulated that females secrete significantly different. The tapping stages chitin- or protein-denaturing enzymes to of ovipositional event I (OEI) and oviposi- dissolve the shell of the ootheca, which is tional event II (OEII) were not signific- thought to accelerate the penetration of antly different either (Table VII). After five the ovipositor. Experienced females pro- days, females forgot what they had learned bably need less time to locate the right spot and acted as inexperience females. for penetration by the ovipositor than do The longevity of E. appendigaster naive females. That is why the preovi- adults in the laboratory has been reported position quiescent stage of experienced to be 13.3 days for females and 14.9 days females was shorter than that of naive for males (Yeh and Mu, 1994a). By offering females in this study. 10% table sugar solution, both males and The preoviposition host contact stage females could survive for more than 30 was shorter in the experienced female in days. Even 12-day-old wasps in the 9th three ovipositions with one day intervals experiment were not treated as old wasps (Table 2). In the host contact stage, the under the laboratory rearing conditions. female drumson the ootheca with its an- The experienced ensign wasp probed tennae consistently (Yeh and Mu, 1994a). using her ovipositor, but some (ca.10%) Antennae drumming is probably for host could not penetrate the ootheca, or the identification. Experienced females need ovipositor was not ready for probing due to less time for host identification. The host morphological damage to the ovipositor contact stage was also shorter in the ex- and the stylets. Such wasps tried to drill perienced female in ovipostional event II but failed to penetrate the oothecae and (OEII). But after five days, the host contact left, terminating the oviposition behavior. stage of ovipositional event II (OEII) and Those that terminated the oviposition ovipositional event III (OEIII) were not behaviors were not counted in this study.

Prior Experience Affects Oviposition Behavior in E. appendigaster 19 Papaj, D. R., and R. J. Prokopy. 1989. Acknowledgments Ecological and evolutionary aspects of learning in phytophagous . We would like to express our thanks to Ann. Rev. Entomol. 34: 315-50. Dr. Eric Jeng, of the Tropical Fruit & SAS. 1988. SAS User’s Guide, Release 4 Research Laboratory, USDA, and Ms. Edition, SAS Institute Inc., Cary, NC. Cheryl Robbins, of the National Museum Townes, H. 1949. The Nearctic species of of Natural Science, Taichung, Taiwan, for Evaniidae. Proc. U.S. Nat. Mus. 99: their critical reading of this manuscript. 525-539. This work was supported by the EPA of Turlings, T. C. J., F. L. Wackers, L. E. M. Taiwan Provincial Government and the Vet, W. J. Lewis, and J. H. EPA of Executive Yuan. Tumlinson, 1993. Learning of host- finding cues by hymenopterous par- References asitoids. In D. R. Papaj and A. C. Lewis (eds.), Insect Learning. Chap- Arthur, A. P. 1971. Associative learning by man & Hal l. pp. 51-78. Nemeritis canescens (Hymenoptera; Vinson, S. B., C. S. Barfield, and, R. D. Ichneumonidae). Can. Entomol. 103: Henson. Oviposition behavior of 1137-1141. Bracon mellitor, a parasitoid of the Carde, R. T., and H. O. Lee. 1989. Effect of boll weevil (Anthonomus grandis ), II. experience on the responses of the Associative learning. Physiol. Entomol. parasitoid Brachymerioa intermedia 2: 157-164. (Hymenoptera: Chalcididae) to its host, Wardle, A. R., and J. H. Borden. 1985. Lymantria dispar (Lepidoptera: Ly- Age-dependency associative learning mantriidae), and to kairomone. Ann. by Exerustes roborator (F.) (Hymen- Entomol. Soc. Am. 82: 653-657. optera: Ichneumonidae). Can. Entomol. Chow, A., and M. Mackauer. 1992. The 117: 605-616. influence of prior ovipositional ex- Wardle, A. R., and J. H. Borden. 1989. perience of host selection in four Learning of an olfactory stimulus species of aphidiid wasps (Hymen- associated with a host-microhabitat optera: Aphidiidae). J. Insect Behav. 5: by Exeristes roborator. Entomol. Exp. 99-108. Zool. 52: 271-279. Lebeck, M. L. 1991. A review of the Wardle, A. R., and J. H. Borden 1991. hymenopterous natural enemies of Effect of prior experience on the cockroaches with emphasis on biolo- response of Exerustes roborator (Hy- gical control. Entomophaga 36: 335- menoptera: Ichneumonidae) to a na- 352. tural host and microhabitat in a se- Lee, H. P., and J. H. Lee. 1989. Oviposition minatural environment. Environ. En- behavior of Ooencyrtus kuvanae (Ho- tomol. 20: 889-898. ward) (Hymenoptera: Encyrtidae), egg Yeh, C. C., and C. C. Mu. 1994a. parasitoid of Lymentria dispar L. Observation of life history of Evania (Lepidoptera: Lymentriidae). Korean J. appendigaster (L.) (Hymenoptera: Ev- Appl. Entomol. 28: 221-228. aniidae) in the laboratory. Chinese J. Lee, H. P., J. H. Lee, and K. S. Ko. 1989. Entomol. 14: 369-378 (in Chinese with Effect of kairomones on host accept- English summary). ance behavior of the parasitoid Bnr- Yeh, C. C., and C. C. Mu. 1994b. achymeria lasus Walker ( Hymenoptera: Observation of the oviposition behav- Chalcididae). Korean J. Entomol. 19: ior of Evania appendigaster (Evaniidae: 267-272. Hymenoptera). Chinese J. Entomol. 14:

20 中華昆蟲第二十卷第一期 463-470 (in Chinese with English Received Aug. 11, 1999 summary). Accepted Dec. 15, 1999

蜚蠊瘦蜂先前產卵經驗影響其產卵行為

葉金彰 黃麒璋 國立中興大學昆蟲學系 臺中市國光路250 號

林政行* 國立自然科學博物館動物學系 臺中市館前路 1 號

摘 要

本文評估蜚蠊瘦蜂(Evania appendigaster (L.))先前產卵經驗對其產卵行為之效 應。先前經驗減少蜚蠊瘦蜂系列產卵行為之時間，產卵前靜止期佔系列產卵行為最 多之時間 ，且亦是最重要的可塑期。如先前產卵經驗超過三天，雌瘦蜂忘記先前所 學，好似未曾有產卵經驗的雌蟲一樣 。重覆先前產卵經驗並不能減少全部系列產卵 行為之時間。

關鍵詞：瘦蜂、美洲蜚蠊、行為、學習。

Prior Experience Affects Oviposition Behavior in E. appendigaster 21